Plant Molecular Biology

, 69:383

Hormone interactions at the root apical meristem

Review

Abstract

Plants exhibit an amazing developmental flexibility. Plant embryogenesis results in the establishment of a simple apical–basal axis represented by apical shoot and basal root meristems. Later, during postembryonic growth, shaping of the plant body continues by the formation and activation of numerous adjacent meristems that give rise to lateral shoot branches, leaves, flowers, or lateral roots. This developmental plasticity reflects an important feature of the plant’s life strategy based on the rapid reaction to different environmental stimuli, such as temperature fluctuations, availability of nutrients, light or water and response resulting in modulation of developmental programs. Plant hormones are important endogenous factors for the integration of these environmental inputs and regulation of plant development. After a period of studies focused primarily on single hormonal pathways that enabled us to understand the hormone perception and signal transduction mechanisms, it became obvious that the developmental output mediated by a single hormonal pathway is largely modified through a whole network of interactions with other hormonal pathways. In this review, we will summarize recent knowledge on hormonal networks that regulate the development and growth of root with focus on the hormonal interactions that shape the root apical meristem.

Keywords

Root meristem Hormonal cross-talk Abscisic acid Auxin Brassinosteroid Cytokinin Ethylene Gibberellin Arabidopsis 

References

  1. Achard P, Vriezen WH, Van Der Straeten D, Harberd NP (2003) Ethylene regulates arabidopsis development via the modulation of DELLA protein growth repressor function. Plant Cell 15:2816–2825. doi:10.1105/tpc.015685 PubMedGoogle Scholar
  2. Achard P, Cheng H, De Grauwe L, Decat J, Schoutteten H, Moritz T, Van Der Straeten D, Peng J, Harberd NP (2006) Integration of plant responses to environmentally activated phytohormonal signals. Science 311:91–94. doi:10.1126/science.1118642 PubMedGoogle Scholar
  3. Aida M, Beis D, Heidstra R, Willemsen V, Blilou I, Galinha C, Nussaume L, Noh YS, Amasino R, Scheres B (2004) The PLETHORA genes mediate patterning of the Arabidopsis root stem cell niche. Cell 119:109–120. doi:10.1016/j.cell.2004.09.018 PubMedGoogle Scholar
  4. Alonso JM, Stepanova AN, Solano R, Wisman E, Ferrari S, Ausubel FM, Ecker JR (2003) Five components of the ethylene-response pathway identified in a screen for weak ethylene-insensitive mutants in Arabidopsis. Proc Natl Acad Sci USA 100:2992–2997. doi:10.1073/pnas.0438070100 PubMedGoogle Scholar
  5. Arteca JM, Arteca RN (2001) Brassinosteroid-induced exaggerated growth in hydroponically grown Arabidopsis plants. Physiol Plant 112:104–112. doi:10.1034/j.1399-3054.2001.1120114.x PubMedGoogle Scholar
  6. Barlier I, Kowalczyk M, Marchant A, Ljung K, Bhalerao R, Bennett M, Sandberg G, Bellini C (2000) The SUR2 gene of Arabidopsis thaliana encodes the cytochrome P450 CYP83B1, a modulator of auxin homeostasis. Proc Natl Acad Sci USA 97:14819–14824. doi:10.1073/pnas.260502697 PubMedGoogle Scholar
  7. Beaudoin N, Serizet C, Gosti F, Giraudat J (2000) Interactions between abscisic acid and ethylene signaling cascades. Plant Cell 12:1103–1115PubMedGoogle Scholar
  8. Beemster GT, Baskin TI (2000) Stunted plant 1 mediates effects of cytokinin, but not of auxin, on cell division and expansion in the root of Arabidopsis. Plant Physiol 124:1718–1727. doi:10.1104/pp.124.4.1718 PubMedGoogle Scholar
  9. Benfey PN, Linstead PJ, Roberts K, Schiefelbein JW, Hauser MT, Aeschbacher RA (1993) Root development in Arabidopsis: four mutants with dramatically altered root morphogenesis. Development 119:57–70PubMedGoogle Scholar
  10. Benjamins R, Quint A, Weijers D, Hooykaas P, Offringa R (2001) The PINOID protein kinase regulates organ development in Arabidopsis by enhancing polar auxin transport. Development 128:4057–4067PubMedGoogle Scholar
  11. Benkova E, Michniewicz M, Sauer M, Teichmann T, Seifertova D, Jurgens G, Friml J (2003) Local, efflux-dependent auxin gradients as a common module for plant organ formation. Cell 115:591–602. doi:10.1016/S0092-8674(03)00924-3 PubMedGoogle Scholar
  12. Bennett MJ, Marchant A, Green HG, May ST, Ward SP, Millner PA, Walker AR, Schulz B, Feldmann KA (1996) Arabidopsis AUX1 gene: a permease-like regulator of root gravitropism. Science 273:948–950. doi:10.1126/science.273.5277.948 PubMedGoogle Scholar
  13. Blakeslee JJ, Bandyopadhyay A, Lee OR, Mravec J, Titapiwatanakun B, Sauer M, Makam SN, Cheng Y, Bouchard R, Adamec J, Geisler M, Nagashima A, Sakai T, Martinoia E, Friml J, Peer WA, Murphy AS (2007) Interactions among PIN-FORMED and P-glycoprotein auxin transporters in Arabidopsis. Plant Cell 19:131–147. doi:10.1105/tpc.106.040782 PubMedGoogle Scholar
  14. Bleecker AB, Kende H (2000) Ethylene: a gaseous signal molecule in plants. Annu Rev Cell Dev Biol 16:1–18. doi:10.1146/annurev.cellbio.16.1.1 PubMedGoogle Scholar
  15. Blilou I, Xu J, Wildwater M, Willemsen V, Paponov I, Friml J, Heidstra R, Aida M, Palme K, Scheres B (2005) The PIN auxin efflux facilitator network controls growth and patterning in Arabidopsis roots. Nature 433:39–44. doi:10.1038/nature03184 PubMedGoogle Scholar
  16. Brocard-Gifford I, Lynch TJ, Garcia ME, Malhotra B, Finkelstein RR (2004) The Arabidopsis thaliana ABSCISIC ACID-INSENSITIVE8 encodes a novel protein mediating abscisic acid and sugar responses essential for growth. Plant Cell 16:406–421. doi:10.1105/tpc.018077 PubMedGoogle Scholar
  17. Camilleri C, Azimzadeh J, Pastuglia M, Bellini C, Grandjean O, Bouchez D (2002) The Arabidopsis TONNEAU2 gene encodes a putative novel protein phosphatase 2A regulatory subunit essential for the control of the cortical cytoskeleton. Plant Cell 14:833–845. doi:10.1105/tpc.010402 PubMedGoogle Scholar
  18. Cano-Delgado A, Yin Y, Yu C, Vafeados D, Mora-Garcia S, Cheng JC, Nam KH, Li J, Chory J (2004) BRL1 and BRL3 are novel brassinosteroid receptors that function in vascular differentiation in Arabidopsis. Development 131:5341–5351. doi:10.1242/dev.01403 PubMedGoogle Scholar
  19. Cary AJ, Liu W, Howell SH (1995) Cytokinin action is coupled to ethylene in its effects on the inhibition of root and hypocotyl elongation in Arabidopsis thaliana seedlings. Plant Physiol 107:1075–1082. doi:10.1104/pp.107.4.1075 PubMedGoogle Scholar
  20. Casson SA, Chilley PM, Topping JF, Evans IM, Souter MA, Lindsey K (2002) The POLARIS gene of Arabidopsis encodes a predicted peptide required for correct root growth and leaf vascular patterning. Plant Cell 14:1705–1721. doi:10.1105/tpc.002618 PubMedGoogle Scholar
  21. Clouse SD, Hall AF, Langford M, Mcmorris TC, Baker ME (1993) Physiological and molecular effects of brassinosteroids on Arabidopsis-Thaliana. J Plant Growth Regul 12:61–66. doi:10.1007/BF00193234 Google Scholar
  22. Cui H, Levesque MP, Vernoux T, Jung JW, Paquette AJ, Gallagher KL, Wang JY, Blilou I, Scheres B, Benfey PN (2007) An evolutionarily conserved mechanism delimiting SHR movement defines a single layer of endodermis in plants. Science 316:421–425. doi:10.1126/science.1139531 PubMedGoogle Scholar
  23. Dello Ioio R, Linhares FS, Scacchi E, Casamitjana-Martinez E, Heidstra R, Costantino P, Sabatini S (2007) Cytokinins determine Arabidopsis root-meristem size by controlling cell differentiation. Curr Biol 17:678–682. doi:10.1016/j.cub.2007.02.047 PubMedGoogle Scholar
  24. Dharmasiri N, Dharmasiri S, Estelle M (2005) The F-box protein TIR1 is an auxin receptor. Nature 435:441–445. doi:10.1038/nature03543 PubMedGoogle Scholar
  25. Di Laurenzio L, Wysocka-Diller J, Malamy JE, Pysh L, Helariutta Y, Freshour G, Hahn MG, Feldmann KA, Benfey PN (1996) The SCARECROW gene regulates an asymmetric cell division that is essential for generating the radial organization of the Arabidopsis root. Cell 86:423–433. doi:10.1016/S0092-8674(00)80115-4 PubMedGoogle Scholar
  26. Dill A, Jung HS, Sun TP (2001) The DELLA motif is essential for gibberellin-induced degradation of RGA. Proc Natl Acad Sci USA 98:14162–14167. doi:10.1073/pnas.251534098 PubMedGoogle Scholar
  27. Dinneny JR, Benfey PN (2008) Plant stem cell niches: standing the test of time. Cell 132:553–557. doi:10.1016/j.cell.2008.02.001 PubMedGoogle Scholar
  28. Dolan L, Janmaat K, Willemsen V, Linstead P, Poethig S, Roberts K, Scheres B (1993) Cellular organisation of the Arabidopsis thaliana root. Development 119:71–84PubMedGoogle Scholar
  29. Eapen D, Barroso ML, Campos ME, Ponce G, Corkidi G, Dubrovsky JG, Cassab GI (2003) A no hydrotropic response root mutant that responds positively to gravitropism in Arabidopsis. Plant Physiol 131:536–546. doi:10.1104/pp.011841 PubMedGoogle Scholar
  30. Eklof S, Astot C, Blackwell J, Moritz T, Olsson O, Sandberg G (1997) Auxin-cytokinin interactions in wild-type and transgenic tobacco. Plant Cell Physiol 38:225–235Google Scholar
  31. Ephritikhine G, Pagant S, Fujioka S, Takatsuto S, Lapous D, Caboche M, Kendrick RE, Barbier-Brygoo H (1999) The sax1 mutation defines a new locus involved in the brassinosteroid biosynthesis pathway in Arabidopsis thaliana. Plant J 18:315–320. doi:10.1046/j.1365-313X.1999.00455.x PubMedGoogle Scholar
  32. Ferreira FJ, Kieber JJ (2005) Cytokinin signaling. Curr Opin Plant Biol 8:518–525. doi:10.1016/j.pbi.2005.07.013 PubMedGoogle Scholar
  33. Fisher RH, Barton MK, Cohen JD, Cooke TJ (1996) Hormonal studies of fass, an Arabidopsis mutant that is altered in organ elongation. Plant Physiol 110:1109–1121PubMedGoogle Scholar
  34. Frigerio M, Alabadi D, Perez-Gomez J, Garcia-Carcel L, Phillips AL, Hedden P, Blazquez MA (2006) Transcriptional regulation of gibberellin metabolism genes by auxin signaling in Arabidopsis. Plant Physiol 142:553–563. doi:10.1104/pp.106.084871 PubMedGoogle Scholar
  35. Friml J, Benkova E, Blilou I, Wisniewska J, Hamann T, Ljung K, Woody S, Sandberg G, Scheres B, Jurgens G, Palme K (2002a) AtPIN4 mediates sink-driven auxin gradients and root patterning in Arabidopsis. Cell 108:661–673. doi:10.1016/S0092-8674(02)00656-6 PubMedGoogle Scholar
  36. Friml J, Wisniewska J, Benkova E, Mendgen K, Palme K (2002b) Lateral relocation of auxin efflux regulator PIN3 mediates tropism in Arabidopsis. Nature 415:806–809PubMedGoogle Scholar
  37. Friml J, Vieten A, Sauer M, Weijers D, Schwarz H, Hamann T, Offringa R, Jurgens G (2003) Efflux-dependent auxin gradients establish the apical–basal axis of Arabidopsis. Nature 426:147–153. doi:10.1038/nature02085 PubMedGoogle Scholar
  38. Fu X, Harberd NP (2003) Auxin promotes Arabidopsis root growth by modulating gibberellin response. Nature 421:740–743. doi:10.1038/nature01387 PubMedGoogle Scholar
  39. Fu X, Richards DE, Ait-Ali T, Hynes LW, Ougham H, Peng J, Harberd NP (2002) Gibberellin-mediated proteasome-dependent degradation of the barley DELLA protein SLN1 repressor. Plant Cell 14:3191–3200. doi:10.1105/tpc.006197 PubMedGoogle Scholar
  40. Fukaki H, Tameda S, Masuda H, Tasaka M (2002) Lateral root formation is blocked by a gain-of-function mutation in the SOLITARY-ROOT/IAA14 gene of Arabidopsis. Plant J 29:153–168. doi:10.1046/j.0960-7412.2001.01201.x PubMedGoogle Scholar
  41. Galinha C, Hofhuis H, Luijten M, Willemsen V, Blilou I, Heidstra R, Scheres B (2007) PLETHORA proteins as dose-dependent master regulators of Arabidopsis root development. Nature 449:1053–1057. doi:10.1038/nature06206 PubMedGoogle Scholar
  42. Galweiler L, Guan C, Muller A, Wisman E, Mendgen K, Yephremov A, Palme K (1998) Regulation of polar auxin transport by AtPIN1 in Arabidopsis vascular tissue. Science 282:2226–2230. doi:10.1126/science.282.5397.2226 PubMedGoogle Scholar
  43. Ghassemian M, Nambara E, Cutler S, Kawaide H, Kamiya Y, McCourt P (2000) Regulation of abscisic acid signaling by the ethylene response pathway in Arabidopsis. Plant Cell 12:1117–1126PubMedGoogle Scholar
  44. Greenboim-Wainberg Y, Maymon I, Borochov R, Alvarez J, Olszewski N, Ori N, Eshed Y, Weiss D (2005) Cross talk between gibberellin and cytokinin: the Arabidopsis GA response inhibitor SPINDLY plays a positive role in cytokinin signaling. Plant Cell 17:92–102. doi:10.1105/tpc.104.028472 PubMedGoogle Scholar
  45. Guo H, Ecker JR (2004) The ethylene signaling pathway: new insights. Curr Opin Plant Biol 7:40–49. doi:10.1016/j.pbi.2003.11.011 PubMedGoogle Scholar
  46. Hamann T, Benkova E, Baurle I, Kientz M, Jurgens G (2002) The Arabidopsis BODENLOS gene encodes an auxin response protein inhibiting MONOPTEROS-mediated embryo patterning. Genes Dev 16:1610–1615. doi:10.1101/gad.229402 PubMedGoogle Scholar
  47. Hardtke CS, Berleth T (1998) The Arabidopsis gene MONOPTEROS encodes a transcription factor mediating embryo axis formation and vascular development. EMBO J 17:1405–1411. doi:10.1093/emboj/17.5.1405 PubMedGoogle Scholar
  48. Hass C, Lohrmann J, Albrecht V, Sweere U, Hummel F, Yoo SD, Hwang I, Zhu T, Schafer E, Kudla J, Harter K (2004) The response regulator 2 mediates ethylene signalling and hormone signal integration in Arabidopsis. EMBO J 23:3290–3302. doi:10.1038/sj.emboj.7600337 PubMedGoogle Scholar
  49. Helariutta Y, Fukaki H, Wysocka-Diller J, Nakajima K, Jung J, Sena G, Hauser MT, Benfey PN (2000) The SHORT-ROOT gene controls radial patterning of the Arabidopsis root through radial signaling. Cell 101:555–567. doi:10.1016/S0092-8674(00)80865-X PubMedGoogle Scholar
  50. Helliwell CA, Sheldon CC, Olive MR, Walker AR, Zeevaart JA, Peacock WJ, Dennis ES (1998) Cloning of the Arabidopsis ent-kaurene oxidase gene GA3. Proc Natl Acad Sci USA 95:9019–9024. doi:10.1073/pnas.95.15.9019 PubMedGoogle Scholar
  51. Hewelt A, Prinsen E, Schell J, Van Onckelen H, Schmulling T (1994) Promoter tagging with a promoterless ipt gene leads to cytokinin-induced phenotypic variability in transgenic tobacco plants:implications of gene dosage effects. Plant J 6:879–891. doi:10.1046/j.1365-313X.1994.6060879.x PubMedGoogle Scholar
  52. Higuchi M, Pischke MS, Mahonen AP, Miyawaki K, Hashimoto Y, Seki M, Kobayashi M, Shinozaki K, Kato T, Tabata S, Helariutta Y, Sussman MR, Kakimoto T (2004) In planta functions of the Arabidopsis cytokinin receptor family. Proc Natl Acad Sci USA 101:8821–8826. doi:10.1073/pnas.0402887101 PubMedGoogle Scholar
  53. Hutchison CE, Li J, Argueso C, Gonzalez M, Lee E, Lewis MW, Maxwell BB, Perdue TD, Schaller GE, Alonso JM, Ecker JR, Kieber JJ (2006) The Arabidopsis histidine phosphotransfer proteins are redundant positive regulators of cytokinin signaling. Plant Cell 18:3073–3087. doi:10.1105/tpc.106.045674 PubMedGoogle Scholar
  54. Chae HS, Faure F, Kieber JJ (2003) The eto1, eto2, and eto3 mutations and cytokinin treatment increase ethylene biosynthesis in Arabidopsis by increasing the stability of ACS protein. Plant Cell 15:545–559. doi:10.1105/tpc.006882 PubMedGoogle Scholar
  55. Chilley PM, Casson SA, Tarkowski P, Hawkins N, Wang KL, Hussey PJ, Beale M, Ecker JR, Sandberg GK, Lindsey K (2006) The POLARIS peptide of Arabidopsis regulates auxin transport and root growth via effects on ethylene signaling. Plant Cell 18:3058–3072. doi:10.1105/tpc.106.040790 PubMedGoogle Scholar
  56. Izhaki A, Swain SM, Tseng TS, Borochov A, Olszewski NE, Weiss D (2001) The role of SPY and its TPR domain in the regulation of gibberellin action throughout the life cycle of Petunia hybrida plants. Plant J 28:181–190. doi:10.1046/j.1365-313X.2001.01144.x PubMedGoogle Scholar
  57. Jasinski S, Piazza P, Craft J, Hay A, Woolley L, Rieu I, Phillips A, Hedden P, Tsiantis M (2005) KNOX action in Arabidopsis is mediated by coordinate regulation of cytokinin and gibberellin activities. Curr Biol 15:1560–1565. doi:10.1016/j.cub.2005.07.023 PubMedGoogle Scholar
  58. Kim GT, Fujioka S, Kozuka T, Tax FE, Takatsuto S, Yoshida S, Tsukaya H (2005) CYP90C1 and CYP90D1 are involved in different steps in the brassinosteroid biosynthesis pathway in Arabidopsis thaliana. Plant J 41:710–721. doi:10.1111/j.1365-313X.2004.02330.x PubMedGoogle Scholar
  59. Knox K, Grierson CS, Leyser O (2003) AXR3 and SHY2 interact to regulate root hair development. Development 130:5769–5777. doi:10.1242/dev.00659 PubMedGoogle Scholar
  60. Kuderova A, Urbankova I, Valkova M, Malbeck J, Nemethova D and Hejatko J (2008) Effects of conditional IPT-dependent cytokinin overproduction on root architecture of Arabidopsis seedlings. Plant Cell Physiol 49:570–582Google Scholar
  61. Kutz A, Muller A, Hennig P, Kaiser WM, Piotrowski M, Weiler EW (2002) A role for nitrilase 3 in the regulation of root morphology in sulphur-starving Arabidopsis thaliana. Plant J 30:95–106. doi:10.1046/j.1365-313X.2002.01271.x PubMedGoogle Scholar
  62. Laplaze L, Benkova E, Casimiro I, Maes L, Vanneste S, Swarup R, Weijers D, Calvo V, Parizot B, Herrera-Rodriguez MB, Offringa R, Graham N, Doumas P, Friml J, Bogusz D, Beeckman T, Bennett M (2007) Cytokinins act directly on lateral root founder cells to inhibit root initiation. Plant Cell 19:3889–3900. doi:10.1105/tpc.107.055863 PubMedGoogle Scholar
  63. Le J, Vandenbussche F, Van Der Straeten D, Verbelen JP (2001) In the early response of Arabidopsis roots to ethylene, cell elongation is up- and down-regulated and uncoupled from differentiation. Plant Physiol 125:519–522. doi:10.1104/pp.125.2.519 PubMedGoogle Scholar
  64. Lee S, Cheng H, King KE, Wang W, He Y, Hussain A, Lo J, Harberd NP, Peng J (2002) Gibberellin regulates Arabidopsis seed germination via RGL2, a GAI/RGA-like gene whose expression is up-regulated following imbibition. Genes Dev 16:646–658. doi:10.1101/gad.969002 PubMedGoogle Scholar
  65. Levesque MP, Vernoux T, Busch W, Cui H, Wang JY, Blilou I, Hassan H, Nakajima K, Matsumoto N, Lohmann JU, Scheres B, Benfey PN (2006) Whole-genome analysis of the SHORT-ROOT developmental pathway in Arabidopsis. PLoS Biol 4:e143. doi:10.1371/journal.pbio.0040143 Google Scholar
  66. Leyser HM, Pickett FB, Dharmasiri S, Estelle M (1996) Mutations in the AXR3 gene of Arabidopsis result in altered auxin response including ectopic expression from the SAUR-AC1 promoter. Plant J 10:403–413. doi:10.1046/j.1365-313x.1996.10030403.x PubMedGoogle Scholar
  67. Li J, Dai X, Zhao Y (2006a) A role for auxin response factor 19 in auxin and ethylene signaling in Arabidopsis. Plant Physiol 140:899–908. doi:10.1104/pp.105.070987 PubMedGoogle Scholar
  68. Li X, Mo X, Shou H, Wu P (2006b) Cytokinin-mediated cell cycling arrest of pericycle founder cells in lateral root initiation of Arabidopsis. Plant Cell Physiol 47:1112–1123. doi:10.1093/pcp/pcj082 PubMedGoogle Scholar
  69. Liang X, Abel S, Keller JA, Shen NF, Theologis A (1992) The 1-aminocyclopropane–1-carboxylate synthase gene family of Arabidopsis thaliana. Proc Natl Acad Sci USA 89:11046–11050. doi:10.1073/pnas.89.22.11046 PubMedGoogle Scholar
  70. Liang Y, Mitchell DM, Harris JM (2007) Abscisic acid rescues the root meristem defects of the Medicago truncatula latd mutant. Dev Biol 304:297–307. doi:10.1016/j.ydbio.2006.12.037 PubMedGoogle Scholar
  71. Luschnig C, Gaxiola RA, Grisafi P, Fink GR (1998) EIR1, a root-specific protein involved in auxin transport, is required for gravitropism in Arabidopsis thaliana. Genes Dev 12:2175–2187. doi:10.1101/gad.12.14.2175 PubMedGoogle Scholar
  72. Mahonen AP, Bonke M, Kauppinen L, Riikonen M, Benfey PN, Helariutta Y (2000) A novel two-component hybrid molecule regulates vascular morphogenesis of the Arabidopsis root. Genes Dev 14:2938–2943. doi:10.1101/gad.189200 PubMedGoogle Scholar
  73. Mahonen AP, Bishopp A, Higuchi M, Nieminen KM, Kinoshita K, Tormakangas K, Ikeda Y, Oka A, Kakimoto T, Helariutta Y (2006) Cytokinin signaling and its inhibitor AHP6 regulate cell fate during vascular development. Science 311:94–98. doi:10.1126/science.1118875 PubMedGoogle Scholar
  74. McGinnis KM, Thomas SG, Soule JD, Strader LC, Zale JM, Sun TP, Steber CM (2003) The Arabidopsis SLEEPY1 gene encodes a putative F-box subunit of an SCF E3 ubiquitin ligase. Plant Cell 15:1120–1130. doi:10.1105/tpc.010827 PubMedGoogle Scholar
  75. Medford JI, Horgan R, El-Sawi Z, Klee HJ (1989) Alterations of Endogenous Cytokinins in Transgenic Plants Using a Chimeric Isopentenyl Transferase Gene. Plant Cell 1:403–413PubMedGoogle Scholar
  76. Miyawaki K, Matsumoto-Kitano M, Kakimoto T (2004) Expression of cytokinin biosynthetic isopentenyltransferase genes in Arabidopsis: tissue specificity and regulation by auxin, cytokinin, and nitrate. Plant J 37:128–138. doi:10.1046/j.1365-313X.2003.01945.x PubMedGoogle Scholar
  77. Mouchel CF, Briggs GC, Hardtke CS (2004) Natural genetic variation in Arabidopsis identifies BREVIS RADIX, a novel regulator of cell proliferation and elongation in the root. Genes Dev 18:700–714. doi:10.1101/gad.1187704 PubMedGoogle Scholar
  78. Mouchel CF, Osmont KS, Hardtke CS (2006) BRX mediates feedback between brassinosteroid levels and auxin signalling in root growth. Nature 443:458–461. doi:10.1038/nature05130 PubMedGoogle Scholar
  79. Muller B and Sheen J (2008) Cytokinin and auxin interaction in root stem-cell specification during early embryogenesis. Nature 453:1094–1097Google Scholar
  80. Mussig C, Shin GH, Altmann T (2003) Brassinosteroids promote root growth in Arabidopsis. Plant Physiol 133:1261–1271. doi:10.1104/pp.103.028662 PubMedGoogle Scholar
  81. Nagpal P, Walker LM, Young JC, Sonawala A, Timpte C, Estelle M, Reed JW (2000) AXR2 encodes a member of the Aux/IAA protein family. Plant Physiol 123:563–574. doi:10.1104/pp.123.2.563 PubMedGoogle Scholar
  82. Nakajima K, Sena G, Nawy T, Benfey PN (2001) Intercellular movement of the putative transcription factor SHR in root patterning. Nature 413:307–311. doi:10.1038/35095061 PubMedGoogle Scholar
  83. Nakamura A, Higuchi K, Goda H, Fujiwara MT, Sawa S, Koshiba T, Shimada Y, Yoshida S (2003) Brassinolide induces IAA5, IAA19, and DR5, a synthetic auxin response element in Arabidopsis, implying a cross talk point of brassinosteroid and auxin signaling. Plant Physiol 133:1843–1853. doi:10.1104/pp.103.030031 PubMedGoogle Scholar
  84. Nishimura C, Ohashi Y, Sato S, Kato T, Tabata S, Ueguchi C (2004) Histidine kinase homologs that act as cytokinin receptors possess overlapping functions in the regulation of shoot and root growth in Arabidopsis. Plant Cell 16:1365–1377. doi:10.1105/tpc.021477 PubMedGoogle Scholar
  85. Nordstrom A, Tarkowski P, Tarkowska D, Norbaek R, Astot C, Dolezal K, Sandberg G (2004) Auxin regulation of cytokinin biosynthesis in Arabidopsis thaliana: a factor of potential importance for auxin-cytokinin-regulated development. Proc Natl Acad Sci USA 101:8039–8044. doi:10.1073/pnas.0402504101 PubMedGoogle Scholar
  86. Okushima Y, Overvoorde PJ, Arima K, Alonso JM, Chan A, Chang C, Ecker JR, Hughes B, Lui A, Nguyen D, Onodera C, Quach H, Smith A, Yu G, Theologis A (2005) Functional genomic analysis of the AUXIN RESPONSE FACTOR gene family members in Arabidopsis thaliana: unique and overlapping functions of ARF7 and ARF19. Plant Cell 17:444–463. doi:10.1105/tpc.104.028316 PubMedGoogle Scholar
  87. Ortega-Martinez O, Pernas M, Carol RJ, Dolan L (2007) Ethylene modulates stem cell division in the Arabidopsis thaliana root. Science 317:507–510. doi:10.1126/science.1143409 PubMedGoogle Scholar
  88. Overvoorde PJ, Okushima Y, Alonso JM, Chan A, Chang C, Ecker JR, Hughes B, Liu A, Onodera C, Quach H, Smith A, Yu G, Theologis A (2005) Functional genomic analysis of the AUXIN/INDOLE–3-ACETIC ACID gene family members in Arabidopsis thaliana. Plant Cell 17:3282–3300. doi:10.1105/tpc.105.036723 PubMedGoogle Scholar
  89. Palni LMS, Burch L, Horgan R (1988) The Effect of Auxin Concentration on Cytokinin Stability and Metabolism. Planta 174:231–234. doi:10.1007/BF00394775 Google Scholar
  90. Paquette AJ, Benfey PN (2005) Maturation of the ground tissue of the root is regulated by gibberellin and SCARECROW and requires SHORT-ROOT. Plant Physiol 138:636–640. doi:10.1104/pp.104.058362 PubMedGoogle Scholar
  91. Petrášek J, Mravec J, Bouchard R, Blakeslee JJ, Abas M, Seifertová D, Wisniewska J, Tadele Z, Kubes M, Covanová M, Dhonukshe P, Skupa P, Benková E, Perry L, Krecek P, Lee OR, Fink GR, Geisler M, Murphy AS, Luschnig C, Zazímalová E, Friml J (2006) PIN proteins perform a rate-limiting function in cellular auxin efflux Science 312:914–918. doi:10.1126/science.1123542 Google Scholar
  92. Pickett FB, Wilson AK, Estelle M (1990) The aux1 Mutation of Arabidopsis Confers Both Auxin and Ethylene Resistance. Plant Physiol 94:1462–1466PubMedGoogle Scholar
  93. Rahman A, Amakawa T, Goto N, Tsurumi S (2001) Auxin is a positive regulator for ethylene-mediated response in the growth of arabidopsis roots. Plant and Cell Physiology 42:301–307. doi:10.1093/pcp/pce035 PubMedGoogle Scholar
  94. Rahman A, Bannigan A, Sulaman W, Pechter P, Blancaflor EB, Baskin TI (2007) Auxin, actin and growth of the Arabidopsis thaliana primary root. Plant J 50:514–528. doi:10.1111/j.1365-313X.2007.03068.x PubMedGoogle Scholar
  95. Rashotte AM, Chae HS, Maxwell BB, Kieber JJ (2005) The interaction of cytokinin with other signals. Physiologia Plantarum 123:184–194. doi:10.1111/j.1399-3054.2005.00445.x Google Scholar
  96. Riefler M, Novak O, Strnad M, Schmulling T (2006) Arabidopsis cytokinin receptor mutants reveal functions in shoot growth, leaf senescence, seed size, germination, root development, and cytokinin metabolism. Plant Cell 18:40–54. doi:10.1105/tpc.105.037796 PubMedGoogle Scholar
  97. Roman G, Lubarsky B, Kieber JJ, Rothenberg M, Ecker JR (1995) Genetic analysis of ethylene signal transduction in Arabidopsis thaliana: five novel mutant loci integrated into a stress response pathway. Genetics 139:1393–1409PubMedGoogle Scholar
  98. Rosado A, Schapire AL, Bressan RA, Harfouche AL, Hasegawa PM, Valpuesta V, Botella MA (2006) The Arabidopsis tetratricopeptide repeat-containing protein TTL1 is required for osmotic stress responses and abscisic acid sensitivity. Plant Physiol 142:1113–1126. doi:10.1104/pp.106.085191 PubMedGoogle Scholar
  99. Ruzicka K, Ljung K, Vanneste S, Podhorska R, Beeckman T, Friml J, Benkova E (2007) Ethylene regulates root growth through effects on auxin biosynthesis and transport-dependent auxin distribution. Plant Cell 19:2197–2212. doi:10.1105/tpc.107.052126 PubMedGoogle Scholar
  100. Sabatini S, Beis D, Wolkenfelt H, Murfett J, Guilfoyle T, Malamy J, Benfey P, Leyser O, Bechtold N, Weisbeek P, Scheres B (1999) An auxin-dependent distal organizer of pattern and polarity in the Arabidopsis root. Cell 99:463–472. doi:10.1016/S0092-8674(00)81535-4 PubMedGoogle Scholar
  101. Sasaki A, Itoh H, Gomi K, Ueguchi-Tanaka M, Ishiyama K, Kobayashi M, Jeong DH, An G, Kitano H, Ashikari M, Matsuoka M (2003) Accumulation of phosphorylated repressor for gibberellin signaling in an F-box mutant. Science 299:1896–1898. doi:10.1126/science.1081077 PubMedGoogle Scholar
  102. Shimada Y, Goda H, Nakamura A, Takatsuto S, Fujioka S, Yoshida S (2003) Organ-specific expression of brassinosteroid-biosynthetic genes and distribution of endogenous brassinosteroids in Arabidopsis. Plant Physiol 131:287–297. doi:10.1104/pp.013029 PubMedGoogle Scholar
  103. Scheres B, Dilaurenzio L, Willemsen V, Hauser MT, Janmaat K, Weisbeek P, Benfey PN (1995) Mutations Affecting the Radial Organization of the Arabidopsis Root Display Specific Defects Throughout the Embryonic Axis. Development 121:53–62Google Scholar
  104. Schlagnhaufer CD, Arteca RN (1985) Brassinosteroid-Induced Epinasty in Tomato Plants. Plant Physiol 78:300–303PubMedCrossRefGoogle Scholar
  105. Sieberer T, Hauser MT, Seifert GJ, Luschnig C (2003) PROPORZ1, a putative Arabidopsis transcriptional adaptor protein, mediates auxin and cytokinin signals in the control of cell proliferation. Curr Biol 13:837–842. doi:10.1016/S0960-9822(03)00327-0 PubMedGoogle Scholar
  106. Smigocki AC (1991) Cytokinin content and tissue distribution in plants transformed by a reconstructed isopentenyl transferase gene. Plant Mol Biol 16:105–115. doi:10.1007/BF00017921 PubMedGoogle Scholar
  107. Son O, Cho HY, Kim MR, Lee H, Lee MS, Song E, Park JH, Nam KH, Chun JY, Kim HJ, Hong SK, Chung YY, Hur CG, Cho HT, Cheon CI (2005) Induction of a homeodomain-leucine zipper gene by auxin is inhibited by cytokinin in Arabidopsis roots. Biochem Biophys Res Commun 326:203–209. doi:10.1016/j.bbrc.2004.11.014 PubMedGoogle Scholar
  108. Stepanova AN, Hoyt JM, Hamilton AA, Alonso JM (2005) A Link between ethylene and auxin uncovered by the characterization of two root-specific ethylene-insensitive mutants in Arabidopsis. Plant Cell 17:2230–2242. doi:10.1105/tpc.105.033365 PubMedGoogle Scholar
  109. Stepanova AN, Yun J, Likhacheva AV, Alonso JM (2007) Multilevel interactions between ethylene and auxin in Arabidopsis roots. Plant Cell 19:2169–2185. doi:10.1105/tpc.107.052068 PubMedGoogle Scholar
  110. Stepanova AN, Robertson-Hoyt J, Yun J, Benavente LM, Xie DY, Dolezal K, Schlereth A, Jurgens G, Alonso JM (2008) TAA1-mediated auxin biosynthesis is essential for hormone crosstalk and plant development. Cell 133:177–191. doi:10.1016/j.cell.2008.01.047 PubMedGoogle Scholar
  111. Swain SM, Tseng TS, Olszewski NE (2001) Altered expression of SPINDLY affects gibberellin response and plant development. Plant Physiol 126:1174–1185. doi:10.1104/pp.126.3.1174 PubMedGoogle Scholar
  112. Swarup R, Perry P, Hagenbeek D, Van Der Straeten D, Beemster GT, Sandberg G, Bhalerao R, Ljung K, Bennett MJ (2007) Ethylene upregulates auxin biosynthesis in Arabidopsis seedlings to enhance inhibition of root cell elongation. Plant Cell 19:2186–2196. doi:10.1105/tpc.107.052100 PubMedGoogle Scholar
  113. Tao Y, Ferrer JL, Ljung K, Pojer F, Hong F, Long JA, Li L, Moreno JE, Bowman ME, Ivans LJ, Cheng Y, Lim J, Zhao Y, Ballare CL, Sandberg G, Noel JP, Chory J (2008) Rapid synthesis of auxin via a new tryptophan-dependent pathway is required for shade avoidance in plants. Cell 133:164–176. doi:10.1016/j.cell.2008.01.049 PubMedGoogle Scholar
  114. Tian Q, Reed JW (1999) Control of auxin-regulated root development by the Arabidopsis thaliana SHY2/IAA3 gene. Development 126:711–721PubMedGoogle Scholar
  115. To JP, Haberer G, Ferreira FJ, Deruere J, Mason MG, Schaller GE, Alonso JM, Ecker JR, Kieber JJ (2004) Type-A Arabidopsis response regulators are partially redundant negative regulators of cytokinin signaling. Plant Cell 16:658–671. doi:10.1105/tpc.018978 PubMedGoogle Scholar
  116. Torres-Ruiz RA, Jurgens G (1994) Mutations in the FASS gene uncouple pattern formation and morphogenesis in Arabidopsis development. Development 120:2967–2978PubMedGoogle Scholar
  117. Tran LS, Urao T, Qin F, Maruyama K, Kakimoto T, Shinozaki K, Yamaguchi-Shinozaki K (2007) Functional analysis of AHK1/ATHK1 and cytokinin receptor histidine kinases in response to abscisic acid, drought, and salt stress in Arabidopsis. Proc Natl Acad Sci USA 104:20623–20628. doi:10.1073/pnas.0706547105 PubMedGoogle Scholar
  118. Truernit E, Siemering KR, Hodge S, Grbic V, Haseloff J (2006) A map of KNAT gene expression in the Arabidopsis root. Plant Mol Biol 60:1–20. doi:10.1007/s11103-005-1673-9 PubMedGoogle Scholar
  119. Tsuchisaka A, Theologis A (2004) Unique and overlapping expression patterns among the Arabidopsis 1-amino-cyclopropane–1-carboxylate synthase gene family members. Plant Physiol 136:2982–3000. doi:10.1104/pp.104.049999 PubMedGoogle Scholar
  120. Ubeda-Tomas S, Swarup R, Coates J, Swarup K, Laplaze L, Beemster GT, Hedden P, Bhalerao R, Bennett MJ (2008) Root growth in Arabidopsis requires gibberellin/DELLA signalling in the endodermis. Nat Cell Biol 10:625–628. doi:10.1038/ncb1726 PubMedGoogle Scholar
  121. Ulmasov T, Murfett J, Hagen G, Guilfoyle TJ (1997) Aux/IAA proteins repress expression of reporter genes containing natural and highly active synthetic auxin response elements. Plant Cell 9:1963–1971PubMedGoogle Scholar
  122. van den Berg C, Weisbeek P, Scheres B (1998) Cell fate and cell differentiation status in the Arabidopsis root. Planta 205:483–491. doi:10.1007/s004250050347 PubMedGoogle Scholar
  123. Vriezen WH, Achard P, Harberd NP, Van Der Straeten D (2004) Ethylene-mediated enhancement of apical hook formation in etiolated Arabidopsis thaliana seedlings is gibberellin dependent. Plant J 37:505–516. doi:10.1046/j.1365-313X.2003.01975.x PubMedGoogle Scholar
  124. Watt FM, Hogan BL (2000) Out of Eden: stem cells and their niches. Science 287:1427–1430. doi:10.1126/science.287.5457.1427 PubMedGoogle Scholar
  125. Weijers D, Benkova E, Jager KE, Schlereth A, Hamann T, Kientz M, Wilmoth JC, Reed JW, Jurgens G (2005) Developmental specificity of auxin response by pairs of ARF and Aux/IAA transcriptional regulators. EMBO J 24:1874–1885. doi:10.1038/sj.emboj.7600659 PubMedGoogle Scholar
  126. Weijers D, Schlereth A, Ehrismann JS, Schwank G, Kientz M, Jurgens G (2006) Auxin triggers transient local signaling for cell specification in Arabidopsis embryogenesis. Dev Cell 10:265–270. doi:10.1016/j.devcel.2005.12.001 PubMedGoogle Scholar
  127. Welch D, Hassan H, Blilou I, Immink R, Heidstra R, Scheres B (2007) Arabidopsis JACKDAW and MAGPIE zinc finger proteins delimit asymmetric cell division and stabilize tissue boundaries by restricting SHORT-ROOT action. Genes Dev 21:2196–2204. doi:10.1101/gad.440307 PubMedGoogle Scholar
  128. Wen CK, Chang C (2002) Arabidopsis RGL1 encodes a negative regulator of gibberellin responses. Plant Cell 14:87–100. doi:10.1105/tpc.010325 PubMedGoogle Scholar
  129. Werner T, Motyka V, Laucou V, Smets R, Van Onckelen H, Schmulling T (2003) Cytokinin-deficient transgenic Arabidopsis plants show multiple developmental alterations indicating opposite functions of cytokinins in the regulation of shoot and root meristem activity. Plant Cell 15:2532–2550. doi:10.1105/tpc.014928 PubMedGoogle Scholar
  130. Wilson AK, Pickett FB, Turner JC, Estelle M (1990) A dominant mutation in Arabidopsis confers resistance to auxin, ethylene and abscisic acid. Mol Gen Genet 222:377–383. doi:10.1007/BF00633843 PubMedGoogle Scholar
  131. Yanai O, Shani E, Dolezal K, Tarkowski P, Sablowski R, Sandberg G, Samach A, Ori N (2005) Arabidopsis KNOXI proteins activate cytokinin biosynthesis. Curr Biol 15:1566–1571. doi:10.1016/j.cub.2005.07.060 PubMedGoogle Scholar
  132. Yang SF, Hoffman NE (1984) Ethylene Biosynthesis and Its Regulation in Higher-Plants. Annual Review of Plant Physiology and Plant Molecular Biology 35:155–189. doi:10.1146/annurev.arplant.35.1.155 Google Scholar
  133. Yang S, Yu H, Xu Y, Goh CJ (2003) Investigation of cytokinin-deficient phenotypes in Arabidopsis by ectopic expression of orchid DSCKX1. FEBS Lett 555:291–296. doi:10.1016/S0014-5793(03)01259-6 PubMedGoogle Scholar
  134. Yang Y, Hammes UZ, Taylor CG, Schachtman DP, Nielsen E (2006) High-affinity auxin transport by the AUX1 influx carrier protein. Curr Biol 16:1123–1127PubMedGoogle Scholar
  135. Yi HC, Joo S, Nam KH, Lee JS, Kang BG, Kim WT (1999) Auxin and brassinosteroid differentially regulate the expression of three members of the 1-aminocyclopropane-1-carboxylate synthase gene family in mung bean (Vigna radiata L.). Plant Mol Biol 41:443–454. doi:10.1023/A:1006372612574 PubMedGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2008

Authors and Affiliations

  1. 1.Department of Plant Systems Biology, Flanders Institute for Biotechnology (VIB)Gent UniversityGentBelgium
  2. 2.Laboratory of Molecular Plant Physiology, Department of Functional Genomics and Proteomics, Institute of Experimental BiologyMasaryk UniversityKamenice 5Czech Republic

Personalised recommendations